Isospora ticoticoi n. sp. (Apicomplexa: Eimeriidae) from the Rufouscollared Sparrow Zonotrichia capensis in South America
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1 Acta Protozoologica Acta Protozool. (2009) 48: Isospora ticoticoi n. sp. (Apicomplexa: Eimeriidae) from the Rufouscollared Sparrow Zonotrichia capensis in South America Lianna M. C. BALTHAZAR 1, Bruno P. BERTO 1, Walter FLAUSINO 2 & Carlos W. G. LOPES 2 1 Curso de Pós-Graduaçăo em Cięncias Veterinárias, Universidade Federal Rural do Rio de Janeiro (UFRRJ) CAPES and REUNI scholarship; 2 Departamento de Parasitologia Animal, Instituto de Veterinária, UFRRJ, BR-465 km 7, Seropédica, RJ, Brasil CNPq fellowship. Summary. This current study reports a new isosporoid (Apicomplexa: Eimeriidae) species parasitizing rufous-collared sparrows, Zonotrichia capensis, kept in captivity located in the mountainous region of Rio de Janeiro, Brazil. Isospora ticoticoi n. sp. oocysts are spherical to sub-spherical, μm, with smooth, bilayered wall, ~1.2 μm. Micropyle and oocyst residuum are absent, however, sometimes, polar granules are present. Sporocysts are ellipsoidal, μm. Stieda and substieda bodies are present. Sporocyst residuum is present, sporozoites have one refractile body and a nucleus. Key words: Isospora ticoticoi, oocysts, coccidiosis, Passeriformes, Emberizidae, Rio de Janeiro, Brazil. INTRODUCTION * Address for correspondence: Carlos W. G. Lopes, Laboratório de Coccídios e Coccidioses, Projeto Sanidade Animal (Embrapa/ UFRRJ), BR-465 km 7, Seropédica, RJ, Brazil. lopescwg@ufrrj.br / bertobp@ufrrj.br The rufous-collared sparrow, Zonotrichia capensis Muller, 1776, is an emberizid bird found in a wide range of habitats, often near humans, from the extreme southeast of Mexico to Tierra del Fuego, and on the island of Hispaniola. In Brazil, it is a very common cage bird due to its beauty and vocalization (Lougheed and Handford 1992, Sick 1997, CBRO 2007). The Emberizidae family is one of the families with more descriptions of isosporoid coccidian parasites. Until this moment 19 species were described in this family. Brazil has 73 distinct emberizid species catalogued; being that many of these species, or others exotic species, are bred in captivity (CBRO 2007). The current study describes a new Isospora species infecting rufous-collared sparrows, Z. capensis, kept in captivity located in the mountainous region of Rio de Janeiro, Brazil. MATERIAL AND METHODS Fecal samples were collected from ten birds of two distinct breeders of rufous-collared sparrow located in Teresópolis City (22 25 S, W), Rio de Janeiro State, Brazil. Three samples were collected from a first breeder, whereas the rest of the samples were collected from the other breeder. Birds were held in individual
2 346 L. M. C. Balthazar et al. cages; samples were collected immediately after defecation and placed into plastic vials containing potassium dichromate solution 2.5% (K 2 Cr 2 O 7 ) (1:6 w/v). Samples were carried to the Laboratório de Coccídios e Coccidioses located at Universidade Federal Rural do Rio de Janeiro (UFRRJ). Samples were placed in a thin layer (~ 5 mm) of K 2 Cr 2 O 7 2.5% solution in Petri plates, and incubated at C for 10 days or until 70% of oocysts were sporulated. Oocysts were recovered by flotation in Sheather s sugar solution (S.G. 1.20) and microscopically examined using the technique described by Duszynski and Wilber (1997). Morphological observations (micropyle [M], oocyst residuum [OR], polar granule [PG], Stieda body [SB], substieda body [SSB], sporocyst residuum [SR], sporozoite [SZ], refractile body [SRB], nucleus [N]) and measurements, in µm, were performed using a binocular microscope Carl Zeiss with apochromatic oil immersion objective lens and ocular micrometer K-15X PZO (Poland). Line drawings were prepared using a binocular microscope Wild M-20 with drawing tube. Pictures were taken using a digital camera model CD Mavica MVC-CD250 Sony. Size ranges are shown in parenthesis followed by average and shape index (L/W ratio). RESULTS Ten rufous-collared sparrows were examined; two of them shed oocysts in the feces. All the positive samples were originating from the first breeder. Initially, the oocysts were non-sporulated, while 70% sporulated by day four. Isospora ticoticoi n. sp. (Figs 1 a d, 2 a c) Description of sporulated oocyst: Oocyst shape (N = 14): spherical to sub-spherical; number of walls: 2; wall thickness: 1.2 ( ); outer wall smooth, about 2/3 of total thickness; L W: ( ), with shape-index: 1.0 ( ); M and O: absent; PG: usually absent; however, sometimes, a unique spherical granule or scattered granules are present. Description of sporocyst and sporozoites: Sporocyst shape (N = 14): ellipsoidal; L W: ( ); shape-index: 1.6 ( ); SB: present, nipple-like, 1.0 high 2.0 wide; SSB: prominent and compartmentalized; a central and denser portion, 1.5 high 2.4 wide; the outer portion is larger and colorless, 2.2 high 3.8 wide; SR: present; SR characteristics: composed of scattered granules of different sizes; SZ: vermiform with 1 posterior SRB and a N. Type-host: The rufous-collared sparrow, Zonotrichia capensis (Muller, 1776) (Passeriformes: Emberizidae). Type-locality: Teresópolis City (22 25 S; W), Rio de Janeiro, Brazil. Material deposited: Oocysts stored in 10% aqueous buffered formalin (v/v), and deposited in the Parasitology Collection, in the Department of Animal Parasitology, at UFRRJ, located in Seropédica, Rio de Janeiro, Brazil. Phototypes and line drawings are deposited at the same location. The repository number is P-34/2009 Site of infection: Unknown. Oocysts collected from fecal samples. Prevalence: 20% (Two of ten examined birds). Etymology: The specific epitaph is derived from the common local name for the host, which is tico-tico. DISCUSSION In spite of Z. capensis to be a very common cage bird in Brazil, the native birds are protected by law. Thus, the breeders make difficult the collect and, for that reason, only ten fecal samples could be collected. Descriptions of isosporan coccidia parasitizing birds of the Emberizidae are frequent. Boughton et al. (1938) recovered oocysts from feces of 13 emberizid species, including the golden-crowned sparrow Z. atricapilla Gmelin, Hadley (1910) reports a coccidium parasitizing the white-throated sparrow Z. albicollis Gmelin, These oocysts, however, were not described or named. Isospora emberizae Mandal, Chakravarty, 1964 was described from the red-headed bunting Emberiza bruniceps Brandt, Isospora exigua McQuistion, Wilson, 1988, I. fragmenta McQuistion, Wilson, 1988, I. rotunda McQuistion, Wilson, 1988 and I. temeraria McQuistion, Wilson, 1988 parasites the small tree-finch Camarhynchus parvulus Gould, 1837; and I. geospizae McQuistion, Wilson, 1989 and I. daphnensis McQuistion, 1990 were described from the medium ground-finch Geospiza fortis Gould, 1837 (Mandal and Chakravarty 1964; McQuistion and Wilson 1988; 1989, McQuistion 1990). Isospora paroariae Upton, Current, Clubb, 1985 was described from the red-crested cardinal, Paroaria coronata Miller, 1776; and Isospora tiaris Ball, Daszak, 1997 was described from soot grassquit, Tiaris fuliginosa Wied, 1830 (Upton et al. 1985, Ball and Daszak 1997). Carvalho-Filho et al. (2005) identified three new species from the double-collared seedeater, Sporophila caerulescens Vieillot, 1823, from Eastern Brazil: I. sporophilae Carvalho-Filho, Meireles, Ribeiro, Lopes,
3 New Isospora from South America 347 Fig. 1. Line drawings of Isospora ticoticoi, a new coccidium species recovered from the rufous-collared sparrow, Zonotrichia capensis. (a) sporulated oocyst with its respective variations of (b, c, d) Stieda and substieda bodies detached. Scale-bar: 10 µm for oocyst (a); and 5µm for Stieda and substieda bodies (b, c, d) 2005, I. flausinoi Carvalho-Filho, Meireles, Ribeiro, Lopes, 2005 and I. teixeirafilhoi Carvalho-Filho, Meireles, Ribeiro, Lopes, Isospora braziliensis Silva, Literák, Koudela, 2006, I. paranaensis Silva, Literák, Koudela, 2006 and I. curio Silva, Literák, Koudela, 2006 were identified from the lesser seed-finch Oryzoborus angolensis Linnaeus, 1766, from Brazil (Silva et al. 2006). Dolnik and Loonen (2007) described, for the first time, an avian isosporan parasite that succeeds transmission while in the High Arctic: Isospora plectrophenaxia Dolnik, Loonen, 2007, parasitized the snow bunting Plectrophenax nivalis Linnaeus, Recently, Berto et al. (2009a) described three new species from the buffy-fronted seedeater S. frontalis Verreaux, 1869: Isospora frontalis Berto, Balthazar, Flausino, Lopes, 2009, I. teresopoliensis Berto, Balthazar, Flausino, Lopes, 2009 and I. chanchaoi Berto, Balthazar, Flausino, Lopes, According to Duszynski and Wilber (1997), a new coccidian species should be compared in details to coccidian species described in the family of the host. Therefore, I. ticoticoi was compared to the coccidia from the Emberizidae. Isospora ticoticoi oocysts can be easily distinguished due to compartmentalization of the SSB, since that no coccidium parasite of emberezid birds presents this characteristic. Isospora emberizae, whose host, E. bruniceps, is distributed in Asia and Europe; I. exigua, I. fragmenta, I. rotunda and I. temeraria, whose host, C. parvulus, occurs in the Galapagos Islands; and I. geospizae and I. daphnensis, whose host, G. fortis, occurs in the Galapagos Islands. Geographic isolation is considered to be a segregation factor for species of Isospora (McQuistion and Wilson 1988). Isospora ticoticoi has not a compact SR founded in I. paroariae, I. sporophilae, I. flausinoi, I. teixeirafilhoi, I.
4 348 L. M. C. Balthazar et al. paranaensis, I. plectrophenaxia and I. chanchaoi. Isospora tiaris, I. frontalis and I. teresopoliensis oocysts are larger than I. ticoticoi, while I. braziliensis oocysts are lesser. Finally, I. curio not presents SSB. In agreement with Grulet et al. (1982), Berto et al. (2009b), Berto et al. (2009c) and Berto et al. (2009d), some variations in the SB and SSB (Figs 1b d) were observed in the sporocysts of this new species; however, these variations are not sufficient enough to describe another new species. Based on the differential morphological features mentioned in this study, this species described above is therefore considered as new to science, representing the twentieth Isospora species described from the Emberizidae. Acknowledgements. The authors would like to thank to the breeders of rufous-collared sparrows located in Teresópolis City, Rio de Janeiro State, Brazil, for permitting and assisting with the collection of the material. REFERENCES Ball S. J., Daszak P. (1997) Isospora tiaris n. sp. (Apicomplexa: Eimeriidae) from the sooty grassquit (Tiaris fuliginosa), a passeriform bird of South America. J. Parasitol. 83: Berto B. P., Balthazar L. M. C., Flausino W., Lopes C. W. G. (2009a) Three new species of Isospora Schneider, 1881 (Apicomplexa: Eimeriidae) from the buffy-fronted seedeater Sporophila frontalis Verreaux, 1869 (Passeriformes: Emberizidae) from South America. Syst. Parasitol. 73: Berto B. P., Balthazar L. M. C., Flausino W., Lopes, C. W. G. (2009b) New isosporoid coccidian parasites of sayaca tanager, Thraupis sayaca, from South America. Acta Parasitol. 54: Berto B. P., Flausino W., Luz H. B., Ferreira I., Lopes C. W. G. (2009c) Two new Isospora species from Brazilian tanager (Ramphocelus bresilius dorsalis) of South America. Parasitol. Res. Berto B. P., Luz H. B., Flausino W., Ferreira I., Lopes C.W.G. (2009d) New species of Eimeria Schneider, 1875 and Isospora Schneider, 1881 (Apicomplexa: Eimeriidae) from the shortcrested flycatcher Myiarchus ferox (Gmelin) (Passeriformes: Tyrannidae) in South America. Syst. Parasitol. Carvalho-Filho P. R., Meireles G. S., Ribeiro C. T., Lopes C. W. G. (2005) Three new species of Isospora Schneider, 1881 (Apicomplexa: Eimeriidae) from the double-collared seed eater, Sporophila caerulescens (Passeriformes: Emberizidae), from Eastern Brazil. Mem. Inst. Oswaldo Cruz 100: CBRO Lista das aves do Brasil. Comitę Brasileiro de Registros Ornitológicos, Rio de Janeiro Fig. 2. Photographs (a, b, c) of Isospora ticoticoi, a new coccidium species recovered from the rufous-collared sparrow, Zonotrichia capensis. Scale-bar: 10 µm.
5 New Isospora from South America 349 Boughton D. C., Boughton R. B., Volk J. (1938) Avian hosts of the genus Isospora (Coccidiidae). Ohio J. Sci. 38: Dolnik O. V., Loonen, M. J. J. E. (2007) Isospora plectrophenaxia n. sp. (Apicomplexa: Eimeriidae), a new coccidian parasite found in Snow Bunting (Plectrophenax nivalis) nestlings on Spitsbergen. Parasitol. Res. 101: Duszynski D., Wilber P. (1997) A guideline for the preparation of species descriptions in the Eimeridae. J. Parasitol. 83: Grulet O., Landau I., Baccam D. (1982) Les Isospora du Moineau domestique; multiplicite des especes. Ann. Parasitol. Hum. Comp. 57: Hadley P. B. (1910) Coccidiosis in the English sparrow and other wild birds. Zentralbl. Bakteriol. 56: Lougheed S. C., Handford P. (1992) Vocal dialects and the structure of geographic variation in morphological and allozymic characters in the Rufous-collared Sparrow. Zonotrichia capensis. Evolution 46: Mandal A. K., Chakravarty M. M. (1964) Studies on some aspects of avian coccidia [Protozoa: Sporozoa]. 2. Five new species of Isospora Schneider, Proc. Zool. Soc. 17: McQuistion T. E., Wilson M. (1988) Four new species of Isospora from the small tree finch (Camarhynchus parvulus) from the Galapagos Island. J. Protozool. 35: McQuistion T. E., Wilson M. (1989) Isospora geospizae, a new coccidian parasite (Apicomplexa: Eimeriidae) from the small ground finch (Geospiza fuliginosa) and the medium ground finch (Geospiza fortis) from the Galapagos Island. System. Parasitol. 14: McQuistion T. E. (1990) Isospora daphnensis n. sp. (Apicomplexa: Eimeriidae) from the medium ground finch (Geospiza fortis) from the Galapagos Island. J. Parasitol. 76: Sick H. (1997) Ornitologia Brasileira. Nova Fronteira, Rio de Janeiro Silva E. A. T., Literák I., Koudela B. (2006) Three new species of Isospora Schneider, 1881 (Apicomplexa: Eimeriidae) from the lesser seed-fich, Oryzoborus angolensis (Passeriformes: Emberizidae) from Brazil. Mem. Inst. Oswaldo Cruz 101: Upton S. J., Current W. L., Clubb S. L. (1985) Two new species of Isospora (Apicomplexa: Eimeriidae) form passeriform birds of South America. System. Parasitol. 7:
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